Wood-Derived Dietary Fibers Promote Beneficial Human Gut Microbiota

ABSTRACT Woody biomass is a sustainable and virtually unlimited source of hemicellulosic polysaccharides. The predominant hemicelluloses in softwood and hardwood are galactoglucomannan (GGM) and arabinoglucuronoxylan (AGX), respectively. Based on the structure similarity with common dietary fibers,...

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Autores principales: Sabina Leanti La Rosa, Vasiliki Kachrimanidou, Fanny Buffetto, Phillip B. Pope, Nicholas A. Pudlo, Eric C. Martens, Robert A. Rastall, Glenn R. Gibson, Bjørge Westereng
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Publicado: American Society for Microbiology 2019
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spelling oai:doaj.org-article:6cb11c5a702c4ecfab9e7e00e54376312021-11-15T15:22:04ZWood-Derived Dietary Fibers Promote Beneficial Human Gut Microbiota10.1128/mSphere.00554-182379-5042https://doaj.org/article/6cb11c5a702c4ecfab9e7e00e54376312019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00554-18https://doaj.org/toc/2379-5042ABSTRACT Woody biomass is a sustainable and virtually unlimited source of hemicellulosic polysaccharides. The predominant hemicelluloses in softwood and hardwood are galactoglucomannan (GGM) and arabinoglucuronoxylan (AGX), respectively. Based on the structure similarity with common dietary fibers, GGM and AGX may be postulated to have prebiotic properties, conferring a health benefit on the host through specific modulation of the gut microbiota. In this study, we evaluated the prebiotic potential of acetylated GGM (AcGGM) and highly acetylated AGX (AcAGX) obtained from Norwegian lignocellulosic feedstocks in vitro. In pure culture, both substrates selectively promoted the growth of Bifidobacterium, Lactobacillus, and Bacteroides species in a manner consistent with the presence of genetic loci for the utilization of β-manno-oligosaccharides/β-mannans and xylo-oligosaccharides/xylans. The prebiotic potential of AcGGM and AcAGX was further assessed in a pH-controlled batch culture fermentation system inoculated with healthy adult human feces. Results were compared with those obtained with a commercial fructo-oligosaccharide (FOS) mixture. Similarly to FOS, both substrates significantly increased (P < 0.05) the Bifidobacterium population. Other bacterial groups enumerated were unaffected with the exception of an increase in the growth of members of the Bacteroides-Prevotella group, Faecalibacterium prausnitzii, and clostridial cluster IX (P < 0.05). Compared to the other substrates, AcGGM promoted butyrogenic fermentation whereas AcAGX was more propiogenic. Although further in vivo confirmation is necessary, these results demonstrate that both AcGGM and AcAGX from lignocellulosic feedstocks can be used to direct the promotion of beneficial bacteria, thus exhibiting a promising prebiotic ability to improve or restore gut health. IMPORTANCE The architecture of the gut bacterial ecosystem has a profound effect on the physiology and well-being of the host. Modulation of the gut microbiota and the intestinal microenvironment via administration of prebiotics represents a valuable strategy to promote host health. This work provides insights into the ability of two novel wood-derived preparations, AcGGM and AcAGX, to influence human gut microbiota composition and activity. These compounds were selectively fermented by commensal bacteria such as Bifidobacterium, Bacteroides-Prevotella, F. prausnitzii, and clostridial cluster IX spp. This promoted the microbial synthesis of acetate, propionate, and butyrate, which are beneficial to the microbial ecosystem and host colonic epithelial cells. Thus, our results demonstrate potential prebiotic properties for both AcGGM and AcAGX from lignocellulosic feedstocks. These findings represent pivotal requirements for rationally designing intervention strategies based on the dietary supplementation of AcGGM and AcAGX to improve or restore gut health.Sabina Leanti La RosaVasiliki KachrimanidouFanny BuffettoPhillip B. PopeNicholas A. PudloEric C. MartensRobert A. RastallGlenn R. GibsonBjørge WesterengAmerican Society for Microbiologyarticlecarbohydrate-active enzymesdietary fibersgut microbiotahemicellulosein vitro fecal fermentationprebioticsMicrobiologyQR1-502ENmSphere, Vol 4, Iss 1 (2019)
institution DOAJ
collection DOAJ
language EN
topic carbohydrate-active enzymes
dietary fibers
gut microbiota
hemicellulose
in vitro fecal fermentation
prebiotics
Microbiology
QR1-502
spellingShingle carbohydrate-active enzymes
dietary fibers
gut microbiota
hemicellulose
in vitro fecal fermentation
prebiotics
Microbiology
QR1-502
Sabina Leanti La Rosa
Vasiliki Kachrimanidou
Fanny Buffetto
Phillip B. Pope
Nicholas A. Pudlo
Eric C. Martens
Robert A. Rastall
Glenn R. Gibson
Bjørge Westereng
Wood-Derived Dietary Fibers Promote Beneficial Human Gut Microbiota
description ABSTRACT Woody biomass is a sustainable and virtually unlimited source of hemicellulosic polysaccharides. The predominant hemicelluloses in softwood and hardwood are galactoglucomannan (GGM) and arabinoglucuronoxylan (AGX), respectively. Based on the structure similarity with common dietary fibers, GGM and AGX may be postulated to have prebiotic properties, conferring a health benefit on the host through specific modulation of the gut microbiota. In this study, we evaluated the prebiotic potential of acetylated GGM (AcGGM) and highly acetylated AGX (AcAGX) obtained from Norwegian lignocellulosic feedstocks in vitro. In pure culture, both substrates selectively promoted the growth of Bifidobacterium, Lactobacillus, and Bacteroides species in a manner consistent with the presence of genetic loci for the utilization of β-manno-oligosaccharides/β-mannans and xylo-oligosaccharides/xylans. The prebiotic potential of AcGGM and AcAGX was further assessed in a pH-controlled batch culture fermentation system inoculated with healthy adult human feces. Results were compared with those obtained with a commercial fructo-oligosaccharide (FOS) mixture. Similarly to FOS, both substrates significantly increased (P < 0.05) the Bifidobacterium population. Other bacterial groups enumerated were unaffected with the exception of an increase in the growth of members of the Bacteroides-Prevotella group, Faecalibacterium prausnitzii, and clostridial cluster IX (P < 0.05). Compared to the other substrates, AcGGM promoted butyrogenic fermentation whereas AcAGX was more propiogenic. Although further in vivo confirmation is necessary, these results demonstrate that both AcGGM and AcAGX from lignocellulosic feedstocks can be used to direct the promotion of beneficial bacteria, thus exhibiting a promising prebiotic ability to improve or restore gut health. IMPORTANCE The architecture of the gut bacterial ecosystem has a profound effect on the physiology and well-being of the host. Modulation of the gut microbiota and the intestinal microenvironment via administration of prebiotics represents a valuable strategy to promote host health. This work provides insights into the ability of two novel wood-derived preparations, AcGGM and AcAGX, to influence human gut microbiota composition and activity. These compounds were selectively fermented by commensal bacteria such as Bifidobacterium, Bacteroides-Prevotella, F. prausnitzii, and clostridial cluster IX spp. This promoted the microbial synthesis of acetate, propionate, and butyrate, which are beneficial to the microbial ecosystem and host colonic epithelial cells. Thus, our results demonstrate potential prebiotic properties for both AcGGM and AcAGX from lignocellulosic feedstocks. These findings represent pivotal requirements for rationally designing intervention strategies based on the dietary supplementation of AcGGM and AcAGX to improve or restore gut health.
format article
author Sabina Leanti La Rosa
Vasiliki Kachrimanidou
Fanny Buffetto
Phillip B. Pope
Nicholas A. Pudlo
Eric C. Martens
Robert A. Rastall
Glenn R. Gibson
Bjørge Westereng
author_facet Sabina Leanti La Rosa
Vasiliki Kachrimanidou
Fanny Buffetto
Phillip B. Pope
Nicholas A. Pudlo
Eric C. Martens
Robert A. Rastall
Glenn R. Gibson
Bjørge Westereng
author_sort Sabina Leanti La Rosa
title Wood-Derived Dietary Fibers Promote Beneficial Human Gut Microbiota
title_short Wood-Derived Dietary Fibers Promote Beneficial Human Gut Microbiota
title_full Wood-Derived Dietary Fibers Promote Beneficial Human Gut Microbiota
title_fullStr Wood-Derived Dietary Fibers Promote Beneficial Human Gut Microbiota
title_full_unstemmed Wood-Derived Dietary Fibers Promote Beneficial Human Gut Microbiota
title_sort wood-derived dietary fibers promote beneficial human gut microbiota
publisher American Society for Microbiology
publishDate 2019
url https://doaj.org/article/6cb11c5a702c4ecfab9e7e00e5437631
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